Proton Pump Inhibitor Omeprazole Suppresses Carcinogen-induced Colonic Adenoma Progression to Adenocarcinoma in F344 Rat.


Journal

Cancer prevention research (Philadelphia, Pa.)
ISSN: 1940-6215
Titre abrégé: Cancer Prev Res (Phila)
Pays: United States
ID NLM: 101479409

Informations de publication

Date de publication:
11 2021
Historique:
received: 09 02 2021
revised: 25 05 2021
accepted: 09 07 2021
pubmed: 4 8 2021
medline: 5 4 2022
entrez: 3 8 2021
Statut: ppublish

Résumé

Colorectal cancer causes over 53,000 deaths annually in the United States. Its rising incidences worldwide and particularly in young adults is a major concern. Here, we evaluated the efficacy of omeprazole that is clinically approved for treating acid reflux, to enable its repurposing for colorectal cancer prevention. In the azoxymethane-induced rat colorectal cancer model, dietary omeprazole (250 and 500 ppm) was administered at early adenoma stage (8 weeks after azoxymethane) to assess the progression of early lesions to adenocarcinoma. Administration of omeprazole at 250 or 500 ppm doses led to suppression of total colon adenocarcinoma incidence by 15.7% and 32% (

Identifiants

pubmed: 34341012
pii: 1940-6207.CAPR-21-0057
doi: 10.1158/1940-6207.CAPR-21-0057
doi:

Substances chimiques

Carcinogens 0
Proton Pump Inhibitors 0
Omeprazole KG60484QX9
Azoxymethane MO0N1J0SEN

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, U.S. Gov't, Non-P.H.S.

Langues

eng

Sous-ensembles de citation

IM

Pagination

1009-1020

Subventions

Organisme : NCI NIH HHS
ID : R01 CA213987
Pays : United States

Informations de copyright

©2021 American Association for Cancer Research.

Références

Siegel RL, Miller KD, Fuchs HE, Jemal A. Cancer statistics, 2021. CA Cancer J Clin. 2021;71:7–33.
Bénard F, Barkun AN, Martel M, von Renteln D. Systematic review of colorectal cancer screening guidelines for average-risk adults: summarizing the current global recommendations. World J Gastroenterol. 2018;24:124–38.
Pushpakom S, Iorio F, Eyers PA, Escott KJ, Hopper S, Wells A, et al. Drug repurposing: progress, challenges and recommendations. Nat Rev Drug Discov. 2019;18:41–58.
Bashashati M, Sarosiek I, McCallum RW. Epidemiology and mechanisms of gastroesophageal reflux disease in the elderly: a perspective. Ann N Y Acad Sci. 2016;1380:230–4.
Kuiper JG, van Herk-Sukel MPP, Lemmens V, Kuipers EJ, Herings RMC. Proton pump inhibitors are not associated with an increased risk of colorectal cancer. GastroHep. 2020;2:165–70.
Graham C, Orr C, Bricks CS, Hopman WM, Hammad N, Ramjeesingh R. A retrospective analysis of the role of proton pump inhibitors in colorectal cancer disease survival. Curr Oncol. 2016;23:e583–8.
Ma T, Wu M, Jia S, Yang L. Proton pump inhibitors and the risk of colorectal cancer: a systematic review and meta-analysis of observational studies. Int J Colorectal Dis. 2020;35:2157–69.
De Milito A, Fais S. Proton pump inhibitors may reduce tumour resistance. Expert Opin Pharmacother. 2005;6:1049–54.
Jin UH, Karki K, Kim SB, Safe S. Inhibition of pancreatic cancer Panc1 cell migration by omeprazole is dependent on aryl hydrocarbon receptor activation of JNK. Biochem Biophys Res Commun. 2018;501:751–7.
Jin UH, Lee SO, Pfent C, Safe S. The aryl hydrocarbon receptor ligand omeprazole inhibits breast cancer cell invasion and metastasis. BMC Cancer. 2014;14:498.
Patlolla JM, Zhang Y, Li Q, Steele VE, Rao CV. Anti-carcinogenic properties of omeprazole against human colon cancer cells and azoxymethane-induced colonic aberrant crypt foci formation in rats. Int J Oncol. 2012;40:170–5.
Luciani F, Spada M, De Milito A, Molinari A, Rivoltini L, Montinaro A, et al. Effect of proton pump inhibitor pretreatment on resistance of solid tumors to cytotoxic drugs. J Natl Cancer Inst. 2004;96:1702–13.
Penman ID, el-Omar E, McGregor JR, Hillan KJ, O'Dwyer PJ, McColl KE. Omeprazole inhibits colorectal carcinogenesis induced by azoxymethane in rats. Gut. 1993;34:1559–65.
Madka V, Kumar G, Pathuri G, Zhang Y, Lightfoot S, Asch AS, et al. Bisphosphonates zometa and fosamax synergize with metformin to prevent AOM-induced colon cancer in F344 rat model. Cancer Prev Res. 2020;13:185–94.
Ward JM, Treuting PM. Rodent intestinal epithelial carcinogenesis: pathology and preclinical models. Toxicol Pathol. 2014;42:148–61.
Varghese F, Bukhari AB, Malhotra R, De A. IHC Profiler: an open source plugin for the quantitative evaluation and automated scoring of immunohistochemistry images of human tissue samples. PLoS One. 2014;9:e96801.
Mohammed A, Janakiram NB, Suen C, Stratton N, Lightfoot S, Singh A, et al. Targeting cholecystokinin-2 receptor for pancreatic cancer chemoprevention. Mol Carcinog. 2019;58:1908–18.
Mager LF, Wasmer MH, Rau TT, Krebs P. Cytokine-induced modulation of colorectal cancer. Front Oncol. 2016;6:96.
Guo F, Yuan Y. Tumor necrosis factor alpha-induced proteins in malignant tumors: progress and prospects. Onco Targets Ther. 2020;13:3303–18.
Manzat Saplacan RM, Balacescu L, Gherman C, Chira RI, Craiu A, Mircea PA, et al. The role of PDGFs and PDGFRs in colorectal cancer. Mediators Inflamm. 2017;2017:4708076.
Cannarile MA, Weisser M, Jacob W, Jegg A-M, Ries CH, Rüttinger D. Colony-stimulating factor 1 receptor (CSF1R) inhibitors in cancer therapy. J Immunotherapy Cancer. 2017;5:53.
Ahn JS, Park SM, Eom CS, Kim S, Myung SK. Use of proton pump inhibitor and risk of colorectal cancer: a meta-analysis of observational studies. Korean J Fam Med. 2012;33:272–9.
Nair AB, Jacob S. A simple practice guide for dose conversion between animals and human. J Basic Clin Pharm. 2016;7:27–31.
Lee YY, Jeon HK, Hong JE, Cho YJ, Ryu JY, Choi J-J, et al. Proton pump inhibitors enhance the effects of cytotoxic agents in chemoresistant epithelial ovarian carcinoma. Oncotarget. 2015;6:35040–50.
Udelnow A, Kreyes A, Ellinger S, Landfester K, Walther P, Klapperstueck T, et al. Omeprazole inhibits proliferation and modulates autophagy in pancreatic cancer cells. PLoS One. 2011;6:e20143.
Hao J, Zhang B, Liu B, Lee M, Hao X, Reuhl KR, et al. Effect of alpha-tocopherol, N-acetylcysteine and omeprazole on esophageal adenocarcinoma formation in a rat surgical model. Int J Cancer. 2009;124:1270–5.
Liu W, Li H, Hong SH, Piszczek GP, Chen W, Rodgers GP. Olfactomedin 4 deletion induces colon adenocarcinoma in ApcMin/+ mice. Oncogene. 2016;35:5237–47.
Wang X, Yu Q, Ghareeb WM, Zhang Y, Lu X, Huang Y, et al. Downregulated SPINK4 is associated with poor survival in colorectal cancer. BMC Cancer. 2019;19:1258.
Yu K, Luján R, Marmorstein A, Gabriel S, Hartzell H. Bestrophin-2 mediates bicarbonate transport by goblet cells in mouse colon. J Clin Invest. 2010;120:1722–35.
Ito G, Okamoto R, Murano T, Shimizu H, Fujii S, Nakata T, et al. Lineage-specific expression of bestrophin-2 and bestrophin-4 in human intestinal epithelial cells. PLoS One. 2013;8:e79693.
Ribeiro FR, Paulo P, Costa VL, Barros-Silva JD, Ramalho-Carvalho J, Jerónimo C, et al. Cysteine-rich secretory protein-3 (CRISP3) is strongly up-regulated in prostate carcinomas with the TMPRSS2-ERG fusion gene. PLoS One. 2011;6:e22317.
Liao Q, Kleeff J, Xiao Y, Guweidhi A, Schambony A, Töpfer-Petersen E, et al. Preferential expression of cystein-rich secretory protein-3 (CRISP-3) in chronic pancreatitis. Histol Histopathol. 2003;18:425–33.
Kwon CH, Park HJ, Choi JH, Lee JR, Kim HK, Jo H-J, et al. Snail and serpinA1 promote tumor progression and predict prognosis in colorectal cancer. Oncotarget. 2015;6:20312–26.
Wu T, Li Y, Liu X, Lu J, He X, Wang Q, et al. Identification of high-risk stage II and stage III colorectal cancer by analysis of MMP-21 expression. J Surg Oncol. 2011;104:787–91.
Ghebremariam YT, Cooke JP, Gerhart W, Griego C, Brower JB, Doyle-Eisele M, et al. Pleiotropic effect of the proton pump inhibitor esomeprazole leading to suppression of lung inflammation and fibrosis. J Transl Med. 2015;13:249.
Huo X, Zhang X, Yu C, Zhang Q, Cheng E, Wang DH, et al. In oesophageal squamous cells exposed to acidic bile salt medium, omeprazole inhibits IL-8 expression through effects on nuclear factor-κB and activator protein-1. Gut. 2014;63:1042–52.
Kawajiri K, Kobayashi Y, Ohtake F, Ikuta T, Matsushima Y, Mimura J, et al. Aryl hydrocarbon receptor suppresses intestinal carcinogenesis in ApcMin/+ mice with natural ligands. Proc Natl Acad Sci U S A. 2009;106:13481–6.
Jin U-H, Michelhaugh SK, Polin LA, Shrestha R, Mittal S, Safe S. Omeprazole inhibits glioblastoma cell invasion and tumor growth. Cancers. 2020;12:2097.
Huber V, Camisaschi C, Berzi A, Ferro S, Lugini L, Triulzi T, et al. Cancer acidity: an ultimate frontier of tumor immune escape and a novel target of immunomodulation. Semin Cancer Biol. 2017;43:74–89.
He J, Shi XY, Li ZM, Pan XH, Li ZL, Chen Y, et al. Proton pump inhibitors can reverse the YAP mediated paclitaxel resistance in epithelial ovarian cancer. BMC Mol Cell Biol. 2019;20:49.
Yu J, Wang N, Gong Z, Liu L, Yang S, Chen GG, et al. Cytochrome P450 1A2 overcomes nuclear factor kappa B-mediated sorafenib resistance in hepatocellular carcinoma. Oncogene. 2020;40:492–507.
Falk GW, Buttar NS, Foster NR, Ziegler KLA, DeMars CJ, Romero Y, et al. A combination of esomeprazole and aspirin reduces tissue concentrations of prostaglandin E(2) in patients with Barrett's esophagus. Gastroenterology. 2012;143:917–26.
Yanagihara GR, de Paiva AG, Neto MP, Torres LH, Shimano AC, Louzada MJQ, et al. Effects of long-term administration of omeprazole on bone mineral density and the mechanical properties of the bone. Rev Bras Ortop. 2015;50:232–8.
Yang YX, Lewis JD, Epstein S, Metz DC. Long-term proton pump inhibitor therapy and risk of hip fracture. JAMA. 2006;296:2947–53.
Heysell S, Thomas T, Morrison A, Barry M. Salmonella panamaand acute respiratory distress syndrome in a traveler taking aproton pump inhibitor. J Travel Med. 2008;15:460–3.
Freedberg DE, Lamousé-Smith ES, Lightdale JR, Jin Z, Yang YX, Abrams JA. Use of acid suppression medication is associated with risk for C. difficile infection in infants andchildren: a population-based study. Clin Infect Dis. 2015;61:912–7.
Seto CT, Jeraldo P, Orenstein R, Chia N, DiBaise JK. Prolongeduse of a proton pump inhibitor reduces microbial diversity: implications for Clostridium difficile susceptibility. Microbiome. 2014;2:42.
Dial M. Proton pump inhibitor use and enteric infections. Am J Gastroenterol. 2009;104:S10–6.
Sherwood MW, Melloni C, Jones WS, Washam JB, Hasselblad V, Dolor RJ. Individual proton pump inhibitors and outcomes in patients with coronary artery disease on dual antiplatelet therapy: a systematic review. J Am Heart Assoc. 2015;4:e002245.

Auteurs

Venkateshwar Madka (V)

Center for Cancer Prevention and Drug Development, Hematology-Oncology Section, Department of Medicine, Stephenson Cancer Center, University of Oklahoma Health Sciences Center, Oklahoma City, Oklahoma.

Gaurav Kumar (G)

Center for Cancer Prevention and Drug Development, Hematology-Oncology Section, Department of Medicine, Stephenson Cancer Center, University of Oklahoma Health Sciences Center, Oklahoma City, Oklahoma.

Gopal Pathuri (G)

Center for Cancer Prevention and Drug Development, Hematology-Oncology Section, Department of Medicine, Stephenson Cancer Center, University of Oklahoma Health Sciences Center, Oklahoma City, Oklahoma.

Janani Panneerselvam (J)

Center for Cancer Prevention and Drug Development, Hematology-Oncology Section, Department of Medicine, Stephenson Cancer Center, University of Oklahoma Health Sciences Center, Oklahoma City, Oklahoma.

Yuting Zhang (Y)

Center for Cancer Prevention and Drug Development, Hematology-Oncology Section, Department of Medicine, Stephenson Cancer Center, University of Oklahoma Health Sciences Center, Oklahoma City, Oklahoma.

Vishal Ganta (V)

Center for Cancer Prevention and Drug Development, Hematology-Oncology Section, Department of Medicine, Stephenson Cancer Center, University of Oklahoma Health Sciences Center, Oklahoma City, Oklahoma.

Stanley Lightfoot (S)

Center for Cancer Prevention and Drug Development, Hematology-Oncology Section, Department of Medicine, Stephenson Cancer Center, University of Oklahoma Health Sciences Center, Oklahoma City, Oklahoma.

Ronald Lubet (R)

Division of Cancer Prevention, Chemopreventive Agent Development Research Group, NCI, Rockville, Maryland.

Chen S Suen (CS)

Division of Cancer Prevention, Chemopreventive Agent Development Research Group, NCI, Rockville, Maryland.

Vernon E Steele (VE)

Division of Cancer Prevention, Chemopreventive Agent Development Research Group, NCI, Rockville, Maryland.

Naveena B Janakiram (NB)

Center for Cancer Prevention and Drug Development, Hematology-Oncology Section, Department of Medicine, Stephenson Cancer Center, University of Oklahoma Health Sciences Center, Oklahoma City, Oklahoma.
DoD-VA Extremity Trauma and Amputation Center of Excellence, Bethesda, Maryland.

Altaf Mohammed (A)

Division of Cancer Prevention, Chemopreventive Agent Development Research Group, NCI, Rockville, Maryland.

Chinthalapally V Rao (CV)

Center for Cancer Prevention and Drug Development, Hematology-Oncology Section, Department of Medicine, Stephenson Cancer Center, University of Oklahoma Health Sciences Center, Oklahoma City, Oklahoma. cv-rao@ouhsc.edu.
VA Medical Center, Oklahoma City, Oklahoma.

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